Harmonia axyridis (Coleoptera: Coccinellidae) in Serbia: its presence on aphid-infested plants and co-occurrence with native aphidophagous coccinellids

Harmonia axyridis in Serbia

  • Ivana Jovičić Institute of Pesticides and Environmental Protection, Banatska 31b, 11080 Belgrade
  • Anđa Radonjić University of Belgrade, Faculty of Agriculture, Nemanjina 6, 11080 Belgrade
  • Petar Kljajić Institute of Pesticides and Environmental Protection, Banatska 31b, 11080 Belgrade
  • Goran Andrić Institute of Pesticides and Environmental Protection, Banatska 31b, 11080 Belgrade
  • Marijana Pražić Golić Institute of Pesticides and Environmental Protection, Banatska 31b, 11080 Belgrade
  • Olivera Petrović-Obradović University of Belgrade, Faculty of Agriculture, Nemanjina 6, 11080 Belgrade
Keywords: harlequin ladybird, Coccinellidae, Aphididae, host plants, predatory insects

Abstract


The presence of the invasive coccinellid Harmonia axyridis in aphid colonies on plants, as well as its co-occurrence with native coccinellid predators was studied in the period 2011-2020. Also, its occurrence on fruit plants and grapes was monitored at harvest time. Research was conducted on 41 locations in Serbia. The feeding of this invasive species was recorded on a total of 43 aphid taxa of 25 different genera. It was most frequently present on aphid colonies of the genera Aphis, Brachycaudus and Myzus. The presence of H. axyridis in aphid colonies was recorded on 58 cultivated plant species: 10 fruit, 7 field crop, 5 vegetable
and 16 ornamental species, as well as 20 non-cultivated plants. Harmonia axyridis feeding was also observed on mature fruit plants of cultivated blueberries, nectarine and grapes in representative production areas in Serbia. Nine native coccinellid species were detected in this study: Adalia bipunctata, Adalia decempunctata, Coccinella septempunctata, Hippodamia sp., Hippodamia apicalis, Hippodamia variegata, Hippodamia tredecimpunctata, Hippodamia undecimnotata and Propylea quatuordecimpunctata. Populations of H. axyridis and native coccinellids co-occurred in aphid colonies on many plants, i.e. in 53.45% of all samples. The results inferred that H. axyridis as a predator of numerous aphids on many plants is a useful coccinellid species. However, it may also be considered as a potential pest in fruit and grape production, and a threat to native aphidophagous coccinellids.

References

Adriaens, T., San Martin, G., Hautier, L., Branquart, E., & Maes, D. (2010). Toward a Noah’s Ark for native ladybirds in Belgium. IOBC/WPRS Bulletin, 58, 1-3.

Aebi, A., Brown, P.M., De Clercq, P., Hautier, L., Howe, A., Ingels, B. … Thomas, A. (2011). Detecting arthropod intraguild predation in the field. BioControl, 56(4), 429-440.

Bienkowski, A. O. (2018). Key for identification of the ladybirds (Coleoptera: Coccinellidae) of European Russia and Russian Caucasus (native and alien species). ZooTaxa, 4472(2). doi: 10.20944/ preprints201803.0083.v1

Biranvand, A., Nedvěd, O., Nattier, R., Nepaeva, E., & Haelewaters, D. (2020). Review of the genus Hippodamia (Coleoptera: Coccinellidae) in the Palearctic region. Oriental Insects, 1-12. doi: https:// doi.org/10.1080/00305316.2020.1763871

Blackman, R.L., & Eastop, V.F. (2020). Aphids on the world’s plants: An online identification and information guide. http://www.aphidsonworldsplants.info/

Brown, P.M.J., Adriaens, T., Bathon, H., Cuppen, J., Goldarazena, A., Hagg, T. ... Roy, D.B. (2008). Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl, 53(1), 5-21.

Brown, P.M., Thomas, C.E., Lombaert, E., Jeffries, D.L., Estoup, A., & Handley, L.J.L. (2011). The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. BioControl, 56(4), 623-641.

Brown, P.M., & Roy, H.E. (2018). Native ladybird decline caused by the invasive harlequin ladybird Harmonia axyridis: evidence from a long-term field study. Insect Conservation and Diversity, 11(3), 230-239.

Burgio, G., Santi, F., & Maini, S. (2002). On intra-guild predation and cannibalism in Harmonia axyridis (Pallas) and Adalia bipunctata L. (Coleoptera: Coccinellidae). Biological Control, 24(2), 110-116.

Eastop, V.F., & Van Emden, H.F. (1972). The insect material. In van Emden H.F. (Ed.), Aphid Technology (pp 1-45). London, UK, New York, USA: Academic Press.

Ejbich, K. (2003). Producers in Ontario and northern US bugged by bad odors in wines. The Wine Spectator, 28(2), 16.

Evans, E.W. (2009). Lady beetles as predators of insects other than Hemiptera. Biological Control, 51(2), 255-267.

Honek, A., Brabec, M., Martinková, Z., Dixon, A. F., Pekár, S., & Skuhrovec, J. (2019). Factors determining local and seasonal variation in abundance of Harmonia axyridis (Coleoptera: Coccinellidae) in Central Europe. European Journal of Entomology, 116, 93-101.

Honek, A., Dixon, A. F., Soares, A. O., Skuhrovec, J., & Martinkova, Z. (2017). Spatial and temporal changes in the abundance and compostion of ladybird (Coleoptera: Coccinellidae) communities. Current Opinion in Insect Science, 20, 61-67.

Honek, A., Martinkova, Z., Dixon, A.F., Roy, H.E., & Pekár, S. (2016). Long-term changes in communities of native coccinellids: population fluctuations and the effect of competition from an invasive non-native species. Insect Conservation and Diversity, 9(3), 202-209.

Ibrahimi, H., Mihoci, I., Stanković, V. M., Bukovec, D., & Kučinić, M. (2016). Harmonia axyridis (Pallas, 1773), Newly recorded invasive Species for Albania. Entomological News, 126(2), 128-131.

Jacas, J. A., Urbaneja, A., & Viñuela, E. (2006). History and future of introduction of exotic arthropod biological control agents in Spain: a dilemma? BioControl, 51(1), 1-30.

Jerinić-Prodanović, D., Protić, L., & Mihajlović, L. (2010). Predators and parasitoids of Cacopsylla pyri (L.) (Hemiptera: Psyllidae) in Serbia. Pesticidi i fitomedicina, 25(1), 29-42.

Jovičić, I., Radonjić, A., & Petrović-Obradović, O. (2016). Aphids (Hemiptera: Aphididae) on alfalfa and their coccinellid predators in Serbia: seasonal abundance. Acta zoologica bulgarica, 68(4), 581- 587.

Katsoyannos, P., Kontodimas, D. C., Stathas, G. J., & Tsartsalis, C. T. (1997). Establishment of Harmonia axyridis on citrus and some data on its phenology in Greece. Phytoparasitica, 25(3), 183- 191.

Koch, R.L. (2003). The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. Journal of Insect Science, 3(1).

Koch, R. L., & Galvan, T. L. (2008). Bad side of a good beetle: the North American experience with Harmonia axyridis. In From biological control to invasion: the ladybird Harmonia axyridis as a model species (pp. 23-35). Dordrecht, Netherlands: Springer.

Koch, R.L., Venette, R.C., & Hutchison, W.D. (2006). Invasions by Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in the western hemisphere: implications for South America. Neotropical Entomology, 35(4), 421-434.

Kulijer, D. (2010). First record of invasive species Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) in Bosnia and Herzegovina. Acta Entomologica Serbica, 15(1), 141-143.

Kulijer, D. (2016). Leptoglossus occidentalis (Heteroptera: Coreidae) and Harmonia axyridis (Coleoptera: Coccinellidae), two new invasive alien species for insect fauna of Macedonia. Ecologica Montenegrina, 5, 22-25.

Marko, V., & Pozsgai, G. (2009). Spread of harlequin ladybird (Harmonia axyridis Pallas, 1773) (Coleoptera, Coccinellidae) in Hungary, and the first records from Romania and Ukraine. Növényvédelem, 45(9), 481-490.

Marković, Č., Stojanović, A., & Dobrosavljević, J. (2018). Diversity and abundance of coccinellids (Coleoptera: Coccinellidae) on trees in parks and tree rows of Belgrade. Biologia, 73(9), 857-865.

Merkl, O. (2008). First record of the harlequin ladybird (Harmonia axyridis Pallas) in Hungary (Coleoptera: Coccinellidae). Növényvédelem, 44(5), 239-242.

Mičetić Stanković V., Koren, T., & Stanković, I. (2011). The Harlequin ladybird continues to invade southeastern Europe. Biological Invasions, 13(8), 1711-1716.

Obrycki, J.J., Harwood, J.D., Kring, T.J., & O’Neil, R.J. (2009). Aphidophagy by Coccinellidae: application of biological control in agroecosystems. Biological Control, 51(2), 244-254.

Orlova-Bienkowskaja, M.J., Ukrainsky, A.S., & Brown, P.M. (2015). Harmonia axyridis (Coleoptera: Coccinellidae) in Asia: a re-examination of the native range and invasion to southeastern Kazakhstan and Kyrgyzstan. Biological Invasions, 17(7), 1941-1948.

Petrović-Obradović, O., Vukašinović, D., Vučetić, A., Milovanović, P., & Krnjajić, S. (2009). Aphis spiraecola Patch. - new pest of apple in Serbia. Biljni lekar (Plant Doctor), 37(1), 7-10.

Petrović-Obradović, O., Ilić-Milošević, M., Stanković, S. S., & Žikić, V. (2020). Nine species of aphids (Hemiptera: Aphididae) new to the fauna of Serbia. Acta Entomologica Serbica, 25(1), 13-19.

Petrović-Obradović, O., Jovičić, I., & Radonjić, A. (2016). Aphids (Hemiptera: Aphididae) on wheat. Biljni lekar (Plant Doctor), 44(5-6), 500-505.

Ratcliffe, S. (2002). National pest alert: Multicolored Asian lady beetle. Washington, USA: USDA CSREES Regional Integrated Pest Management Program and the Pest Management Centers.

Roy, H., & Migeon, A. (2010). Ladybeetles (Coccinellidae). Chapter 8.4. BioRisk, 4, 293.

Thalji, R. (1994). Occurrence and distribution of aphidophagous coccinellids (Coleoptera: Coccinellidae) on agricultural crops and wild plants in Vojvodina (Yugoslavia). Zastita bilja (Yugoslavia), 210, 271-291.

Thalji, R., & Stojanović, D. (2008). First sighting of the invasive ladybird Harmonia axyridis Pallas (Coleoptera, Coccinellidae) in Serbia. Biljni lekar (Plant Doctor), 36(6), 389-393.

Tomov, R., Trencheva, K., Trenchev, G., & Kenis, M. (2009). The multicolored invasive Asian ladybird Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) new to the fauna of Bulgaria. Acta Zoologica Bulgarica, 61, 307-311.

Vandereycken, A., Durieux, D., Joie, É., Haubruge, É., & Verheggen, F. (2012). Habitat diversity of the multicolored Asian ladybeetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in agricultural and arboreal ecosystems: a review. Biotechnologie, Agronomie, Societé et Environnement, 16(4), 553-563.

Vandereycken, A., Brostaux, Y., Joie, E., Haubruge, E., & Verheggen, F. J. (2013). Occurrence of Harmonia axyridis (Coleoptera: Coccinellidae) in field crops. European Journal of Entomology, 110(2), 285-292.

Vučetić, A., Petrović-Obradović, O., & Vukašinović, D. (2010). Aphids (Aphididae, Hemiptera) of stone fruit trees. Biljni lekar (Plant Doctor), 38(4/5), 347-354.

Published
2021/03/09
How to Cite
Jovičić, I., Radonjić, A., Kljajić, P., Andrić, G., Pražić Golić, M., & Petrović-Obradović, O. (2021). Harmonia axyridis (Coleoptera: Coccinellidae) in Serbia: its presence on aphid-infested plants and co-occurrence with native aphidophagous coccinellids. Pesticides and Phytomedicine / Pesticidi I Fitomedicina, 35(3), 145-159. https://doi.org/10.2298//PIF2003145J
Section
Original Scientific Paper